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Aquatic Invasions (2010) Volume 5, Supplement 1: S27-S30 This is an Open Access article; doi: 10.3391/ai.2010.5.S1.007 Open Access © 2010 The Author(s). Journal compilation © 2010 REABIC

Aquatic Invasions Records

Establishment of the angular rhomboides (Linnaeus, 1758) (Crustacea, , Brachyura) in the southern

Hermann Neumann1*, Siegfried Ehrich2 and Ingrid Kröncke1 1Senckenberg Institute, Department for Marine Research, Südstrand 40, 26382 Wilhelmshaven, Germany 2Federal Research Institute for Rural Areas, Forestry and Fisheries, Palmaille 9, 22767 Hamburg, Germany E-mail: [email protected] (HN), [email protected] (SE), [email protected] (IK) * Corresponding author

Received: 8 April 2010 / Accepted: 21 May 2010 / Published online: 31 May 2010

Abstract

So far the angular crab (Linnaeus, 1758) was mostly a northeastern Atlantic and Mediterranean and was quite rare in the North Sea where no evidence for sustainable populations existed. In 2008 and 2009 a total of 82 individuals of Goneplax rhomboides (Linnaeus, 1758) were found at 22 widespread locations in the southern North Sea indicating that this species is now well established in the area.

Key words: Goneplax rhomboides, North Sea, alien species, range extension, climate change, larvae drift, currents

Introduction 1963 (73 m), from the Doggerbank in 1998 (NW Rough, 54 m, sand and gravel) and from Smiths The angular crab Goneplax rhomboides is a Knoll in 2000 (Yarmouth area, 30 m) (Moore brachyuran crab with a distinctive rectangular 1987; d'Udekem d'Acoz 2001). More recently, carapax whose color varies from yellow to red. G. rhomboides was found in Dutch waters Carapax of typical male is 20 mm in length and (Ruijter 2004; Oosterbaan 2005) where it was 34 mm in breadth, those of female 11 mm and 18 caught regularly since 2004 during scientific mm, respectively (Moyse and Smaldon 1990). A surveys in the Oyster Ground with an 8 m beam clear sexual dimorphism is obvious in chelipeds trawl (I. de Boois, pers. comm.). Additionally, a length with chelipeds of males four or five times single juvenile of G. rhomboides was found in length of carapax (100 mm) and conspicuous the outside part of the Oslofjord (Norway) at 50 shorter in female (Figure 2 and 3). m depth in 2009 (NIVA 2009). Goneplax rhomboides is native to the north- eastern Atlantic (Türkay 1976; Farina et al. 1997; Trenkel et al. 2007) where it is fairly Materials and methods common on all British coasts (Skewes 2008) as well as in the Mediterranean where it is frequent Samples were taken during scientific surveys in and common from 3 to 750 m on muddy to sandy August 2008 and 2009 as well as in December bottom (Cartes and Sarda 1992; Abello et al. 2009 in the southern North Sea (Figure 1). 2002; Sartor et al. 2006; Fanelli et al. 2007; Samples in August 2008 and 2009 were analysed Balkis and Kurun 2008). The southern from 2 m beam trawl catches during the ICES- distribution limit of G. rhomboides in the eastern coordinated International Bottom Trawl Survey Atlantic is uncertain since West and South (IBTS), which covers an area from 53°30' to African populations of G. rhomboides (e.g. 56°N and 3° to 8°E. Epifauna sampling during Manning and Holthuis 1981) were now regarded this survey took place every year in the summer to be populations of the new species Goneplax months since 1998 and G. rhomboides was found clevai (Guinot and Castro 2007). for the first time in 2008. Additionally, However, G. rhomboides has been very rarely G. rhomboides was caught in December 2009 recorded in the North Sea and no evidence for with a 7 m beam trawl during an epibenthic and sustainable populations existed. Single records demersal fish survey in the German Exclusive were reported from Northumberland coast in Economic Zone (EEZ). This survey started in

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Figure 1. Sampling sites in the southern North Sea. Black triangles, crosses and circles show sampling sites where Goneplax rhomboides was found in August 2008, August 2009 and December 2009, respectively. White triangles, crosses and circles indicate sampling sites where G. rhomboides was not found during these surveys.

Figure 3. Goneplax rhomboides (Linnaeus, 1758): ventral view of male (left) and female (right) clearly showing the sexual dimorphism in chelipeds length. Photograph by H. Neumann.

2004 and samples were taken every December at 83 stations in the German EEZ. G. rhomboides was recorded for the first time at this survey in 2009. All samples were taken during daylight.

Results and discussion

A total number of 82 individuals of the angular crab Goneplax rhomboides (Linnaeus, 1758) Figure 2. Goneplax rhomboides (Linnaeus, 1758): dorsal (Crustacea, Decapoda, Brachyura) were found in view of male (top), female (middle) and juvenile (bottom). Photograph by H. Neumann. depths ranging from 25 m to 50 m on

S28 Establishment of Goneplax rhomboides in the southern North Sea predominant muddy bottom (Annex 1; Figure 1). between G. rhomboides and other burrowing Most locations where G. rhomboides was found species in the southern North Sea such as the as well as highest abundances of G. rhomboides Norway lobster or the were recorded in the German EEZ, where a 7 m masked crab Corystes cassivelaunus (Pennant, beam trawl was used. However, locations and 1777), which were common species in the abundances may be underestimated during our German EEZ. On the other hand Trenkel et al. surveys easterly of the EEZ (Oyster Ground) (2007) found that a temporal separation due to where we used a 2 m beam trawl, since different diurnal activity patterns reduce direct G. rhomboides lives in burrows up to 15 cm competition of G. rhomboides and N. norvegicus beneath the surface (Rice and Chapman 1971) in the Bay of Biscay. and catch efficiency of small beam trawls is low for burrowing species (Reiss et al. 2006). It is Acknowledgements most likely that our 2 m beam trawl data were not representative for the Qyster Ground, since We thank the captains and crews of RV “Walther Herwig III” G. rhomboides was regularly caught in high and “Solea” for their assistance during sampling. The Federal abundances during scientific surveys in that area Research Institute for Rural Areas, Forestry and Fisheries is gratefully acknowledged for providing ship time and data. with an 8 m beam trawl (I. de Boois, pers. The present study was prepared at the Biodiversity and comm.). Additionally, there is evidence that Climate Research Centre (BiK-F), Frankfurt a.M., and finan- G. rhomboides is more active early at night cially supported by the research funding programme “LOEWE (Atkinson and Naylor 1973). Since samples were – Landes-Offensive zur Entwicklung Wissenschaftlich- ökonomischer Exzellenz" of Hesse's Ministry of Higher taken by day during our surveys, this may result Education, Research, and the Arts. Special thanks are due to in an underestimation of records of Stephan Gollasch, Vadim Panov and two anonymous G. rhomboides in the southern North Sea. reviewers for their useful comments on the manuscript. However, sex and carapax length/breadth of G. rhomboides were determined at our surveys in References August 2008 and 2009. In total, we found 10 males and 8 females with a maximum carapax Abello P, Corbera J (1996) Epibiont bryozoans (, length in male of 13 – 22 mm (breadth 21 – 37 Ctenostomatida) of the crab Goneplax rhomboides (Brachyura, ) off the Ebro delta (western mm) and in female of 5 – 16 mm (breadth 9 – 25 Mediterranean). Miscellania Zoologica (Barcelona) 19: mm). At least five individuals were juveniles, 43-52 one female was ovigerous and on the carapax of Abello P, Carbonell A, Torres P (2002) Biogeography of five males the epibiontic bryozoan Triticella epibenthic on the shelf and upper slope off the Iberian Peninsula Mediterranean coasts: implications flava Dalyell, 1848 (Bryozoa, Ctenostomatida) for the establishment of natural management areas. was found, which is a common epibiont of Scientia Marina 66: 183-198 G. rhomboides in the Mediteranean (Abello and Atkinson RJA, Naylor E (1973) Activity rhythms in some Corbera 1996), but also of other such as burrowing decapods. Helgoländer wissenschaftliche Mee- resuntersuchungen 24: 192-201, doi:10.1007/BF01609511 the Norway lobster Nephrops norvegicus Balkis H, Kurun A (2008) The crab species found in the (Linnaeus, 1758) in the North Sea (Ryland Edremit Bay (NE Aegean Sea). Journal of the Black Sea 1990). We hypothesise, that G. rhomboides Mediterranean Environment 14: 39-51 extents its distribution range from the eastern Cartes JE, Sarda F (1992) Abundance and diversity of decapod crustaceans in the deep-catalan sea (western Atlantic to the southern North Sea and is now Mediteranean). Journal of Natural History 26: 1305- well established in that area, which is indicated 1323, doi:10.1080/00222939200770741 by the regular findings of juveniles, ovigerous d'Udekem d'Acoz C (2001) New records of Monodaeus females and individuals of various size. It is couchii (Couch, 1851) and Goneplax rhomboides (Linnaeus, 1758) in the North Sea (Crustacea, Decapoda, reasonable, that larvae of G. rhomboides were Brachyura). Strandvlo 21: 48-50 introduced into the southern North Sea via Fanelli E, Colloca F, Ardizzone G (2007) Decapod channel currents and that an increase in water assemblages off the west coast of central Italy (western temperature especially during the winter months Mediterranean). Scientia Marina 71: 19-28 Farina AC, Freire J, Gonzalez-Gurriaran E (1997) Mega- (Neumann et al. 2009) enhances the survival of benthic decapod crustacean assemblages on the Galician the larvae in that area. However, shipping as continental shelf and upper slope (north-west Spain). potential vector of arrival cannot be excluded. 127: 419-434, doi:10.1007/s002270050029 So far the consequences of the establishment Guinot D, Castro P (2007) A new species of Goneplax Leach, 1814 (Crustacea, Decapoda, Brachyura, Goneplacidae) of G. rhomboides on the benthic communities in from the south Atlantic and the western limits of the Indo- the southern North Sea remain unclear. One West Pacific region, long confused with G. rhomboides might assume a competition especially for space (Linnaeus, 1758). Zootaxa 1577: 17-31

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Manning RB, Holthuis LB (1981) West African brachyuran Rice AL, Chapman CJ (1971) Observations on burrows and crabs (Crustacea: Decapoda). Smithsonian Contributions burrowing behaviour of two mud-dwelling decapod to Zoology 306: i-xii, 1-379 crustaceans, Nephrops norvegicus and Goneplax rhombo- Moore JJ (1987) The marine fauna of the Cullercoast district, ides. Marine Biology 10: 330-342, doi:10.1007/BF00368093 21. Crustacea: Decapoda. Report of the Dove Marine Ruijter Rd (2004) CS-verslag. Het Zeepaard 64: 165-171 Laboratory 34: 1-81 Ryland JS (1990) Lophorate Phyla. In: Hayward PJ, Ryland Moyse J, Smaldon G (1990) Crustacea III: JS (eds) The Marine Fauna of the British Isles and North- Eucarida. In: Hayward PJ, Ryland JS (eds) The Marine West Europe. Clarendon Press, Oxford Fauna of the British Isles and North-West Europe. Sartor P, Francesconi B, Rossetti I, De Ranieri S (2006) Catch Clarendon Press, Oxford composition and damage incurred to crabs discarded from Neumann H, Reiss H, Rakers S, Ehrich S, Kröncke I (2009) the eastern Ligurian Sea "rapido" trawl fishery. Hydro- Temporal variability of southern North Sea epifauna biologia 557: 121-133, doi:10.1007/s10750-005-1315-x communities after the cold winter 1995/1996. ICES Skewes M (2008) Marine Biological Association of the Journal of Marine Science 66: 2233-2243, doi:10.1093/ United Kingdom. http://www.marlin.ac.uk/species icesjms/fsp203 information.php?speciesID=3411 (Accessed 18 March 2010) NIVA (2009) Norsk institutt for vannforskning. http://www.ni Trenkel VM, Le Loc'h F, Rochet MJ (2007) Small-scale va.no/symfoni/infoportal/publikasjon.nsf/.vieInterForsideNIVA spatial and temporal interactions among benthic /A653808EA78B96A9C125764300444397?OpenDocument&Ca crustaceans and one fish species in the Bay of Biscay. tegory=&m1=Nyheter (Accessed 19 May 2010) Marine Biology 151: 2207-2215, doi:10.1007/s00227-007- Oosterbaan A (2005) Hoekige krab rukt op [The angular crab 0655-7 is advancing]. Natura (Utrecht) 102: 75 Türkay M (1976) Decapoda Reptantia von der portugiesischen Reiss H, Kröncke I, Ehrich S (2006) Estimating catch und marokkanischen Küste: Auswertungen der Fahrten 8, efficiency of a 2 m beam trawl for sampling epifauna by 9c (1967), 19 (1970), 23 (1971) und 36 (1975) von F.S. removal experiments. ICES Journal of Marine Science "Meteor". In: DFG (ed) "Meteor" Forschungsergebnisse. 63: 1453-1464, doi:10.1016/j.icesjms.2006.06.001 Gebrüder Borntraeder, Berlin, Stuttgart, pp 23-44

Annex 1. Records of Goneplax rhomboides in the southern North Sea.

Fishing Codend Record Record coordinates Year Abundance Depth Gear duration mesh size No. Latitude, °N Longitude, °E [min] [mm] 1 2009 54°59,10' 6°32,93' 10 45 7 m beam trawl 15 20 2 2009 55°08,97' 6°24,89' 6 48 7 m beam trawl 15 20 3 2009 55°20,55' 6°11,37' 5 48 7 m beam trawl 15 20 4 2009 55°12,14' 5°36,21' 1 43 7 m beam trawl 15 20 5 2009 55°40,95' 5°44,09' 1 50 7 m beam trawl 15 20 6 2009 55°30,09' 6°25,57' 3 42 7 m beam trawl 15 20 7 2009 55°23,22' 6°57,04' 8 30 7 m beam trawl 15 20 8 2009 54°25,08' 6°15,19' 4 39 7 m beam trawl 15 20 9 2009 54°16,05' 6°12,81' 3 37 7 m beam trawl 15 20 10 2009 54°28,98' 5°26,15' 1 41 7 m beam trawl 15 20 11 2009 54°50,01' 5°35,03' 1 42 7 m beam trawl 15 20 12 2009 54°58,97' 5°59,43' 14 37 7 m beam trawl 15 20 13 2009 54°44,28' 6°10,97' 3 41 7 m beam trawl 15 20 14 2009 53°56,14' 6°43,27' 1 25 7 m beam trawl 15 20 15 2009 54°44,34' 5°02,34' 2 45 7 m beam trawl 15 20 16 2009 54°53,24' 5°11,02' 1 40 7 m beam trawl 15 20 17 2008 54°36,74' 5°29,21' 2 43 2 m beam trawl 5 4 18 2008 54°34,95' 4°49,70' 7 46 2 m beam trawl 5 4 19 2008 53°51,19' 4°37,22' 2 41 2 m beam trawl 5 4 20 2009 53°51,14' 4°36,05' 4 42 2 m beam trawl 5 4 21 2009 54°48,89' 6°35,53' 2 41 2 m beam trawl 5 4 22 2009 54°48,11' 3°39,95' 1 45 2 m beam trawl 5 4

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